When someone betrays us, how does the brain deal with it? A hormone associated with social attachment gives us clues.

The development of trust is an essential social tool, allowing people to form productive and meaningful relationships, both at a professional and personal level. Bonds of trust are also extremely fragile, however and a single act of betrayal—such as a marital affair—can instantly erase years of trustworthy behavior. The consequences of such breaches in confidence can be disastrous, and not only for a relationship. People who have been betrayed in the past will sometimes start avoiding future social interactions, which is a potential precursor to social phobia. In light of these connections, recent research has attempted to elucidate the neural mechanisms underlying trust behavior. This is the goal of an exciting new study by neuroscientist Thomas Baumgartner and colleagues at the University of Zurich in Switzerland that combines different disciplines (economics and neuroscience) and methodologies (neuroimaging and neuropharmacology) to investigate how the brain adapts to breaches of trust.

The Chemistry of TrustTo study social interactions, economists, and more recently neuroscientists, take advantage of a simple game played between two people called the “trust game.” (For more on greed and altruism, see this.) In a typical trust game, an investor (Player 1) is faced with a decision to keep a sum of money (say, $10) or share it with a trustee (Player 2). If shared, the investment is tripled ($30) and the trustee now faces the decision to repay the trust by sending back a larger amount of the initial investment (for example, $15 for each participant) or to defect and violate trust by keeping the money. In this game, the investor is therefore left with an important social dilemma: to trust or not to trust. Although it is more profitable to trust, doing so leaves the investor at risk of betrayal.

It has been hypothesized that oxytocin, a hormone recognized for its role in social attachment and facilitation of social interactions, is also important in the formation of trust. For instance, application of oxytocin to “investors” in experimental games increases their tendency to engage in social risks and trust someone else with their money (see this and this). The study by Baumgartner and his colleagues highlights the neural mechanisms through which oxytocin acts to facilitate trust behavior by investigating what happens in the brain when trust breaks down.

When Trust Is BrokenThe authors used functional magnetic resonance imaging (fMRI) to scan 49 participants who were given either placebo or oxytocin via a nasal spray. Participants were instructed to act as investors during multiple rounds of a trust game with different trustees. They were also told that they would engage in a risk game (similar to the trust game in terms of financial risk, but played against a computer instead of another human being). In order to investigate the role of oxytocin following breaches of trust, the experiment was divided into a pre- and post-feedback phase. In between the two phases, participants received feedback information indicating that roughly 50 percent of their decisions (in both trust and risk games) had resulted in poor investments—that is, their trust had been breached (trust game) or their gamble did not pay off (risk game).

Participants who were given a placebo prior to playing the game decreased their rate of trust (that is, how much money they were willing to invest) after they discovered their trust had been violated. Participants who received oxytocin, however, continued to invest at similar rates regardless of whether or not their trusting behavior had been taken advantage of. These behavioral group differences were accompanied by differences in neural responses, as participants in the oxytocin group showed decreases in responses in the amygdala and caudate nucleus. The amygdala is a region of the brain involved in emotion and fear learning, and is rich in oxytocin receptors, whereas the caudate nucleus has been previously linked to reward-related responses and learning to trust . Thus, the authors hypothesized that oxytocin decreases both fear mechanisms associated with a potential aversion of betrayals (via the amygdala) and our reliance on positive feedback that can influence future decisions (via the caudate). This in turn facilitates the expression of trust even after breaches of trust have occurred. Notably, the behavioral and neural results observed were only apparent when participants played the trust game, but not the risk game, suggesting that oxytocin’s effects on trust are exclusive to interactions with real people.

A Science of Social Phobias?The study demonstrates how oxytocin can facilitate social interactions after trust has been violated, by potentially lowering defense mechanisms associated with social risks and by overcoming negative feedback that is important for adapting behavior in the future. These intriguing results provide an important step in our understanding of mental disorders where deficits in social behavior are observed. Excessive fear of betrayal, for example, could serve as a precursor to social phobia, a disorder characterized by a disabling fear of social interactions. Over the long-term, this lack of social interaction may lead to serious problems in mental and physical well-being. Thus, to continue forming a bridge between basic and clinical research, future studies may focus on the effects of oxytocin during the sort of betrayals that more commonly occur in real life (such as being betrayed by a loved one or a business partner). It will also be interesting to examine how different genders respond to breaches in confidence following oxytocin administration.

Trust is an adaptive mechanism essential to building social relationships, and breaches of trust have a profound impact on social behavior and mental health. Understanding the balance between levels of oxytocin and appropriate levels of trust will be another important step in the future. Lower levels of oxytocin in some situations may certainly be adaptive, as a person will become more wary of possible harm. Higher levels of oxytocin, however, may also be necessary at times to allow an individual to “forgive and forget,” an imperative step in maintaining long-term relationships and mental well-being.